Functional advantages of Porphyromonas gingivalis vesicles

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Ho, Meng Hsuan ^a   Chen, Chin Ho ^b   Goodwin, J Shawn ^a   Wang, Bing Yan ^c   Xie, Hua ^a  

^a MEHARRY MEDICAL COLLEGE   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL RNA;

ARTICLE; BACTERIAL MEMBRANE; BACTERIAL OUTER MEMBRANE VESICLE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BIOFILM; CELL FUNCTION; CELL INVASION; CONTROLLED STUDY; FIBROBLAST; GINGIVA; HORIZONTAL GENE TRANSFER; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; MOUTH CAVITY; MOUTH EPITHELIUM CELL; NONHUMAN; PORPHYROMONAS GINGIVALIS; STREPTOCOCCUS GORDONII; UMBILICAL VEIN ENDOTHELIAL CELL; BACTERIAL GENE; BACTEROIDACEAE INFECTION; CELL CULTURE; CELL MEMBRANE; EXOSOME; KERATINOCYTE; MICROBIOLOGY; PERIODONTITIS; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); PORPHYROMONAS GINGIVALIS; STREPTOCOCCUS GORDONII;

BACTEROIDACEAE INFECTIONS; BIOFILMS; CELL MEMBRANE; CELLS, CULTURED; EXTRACELLULAR VESICLES; FIBROBLASTS; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; KERATINOCYTES; PERIODONTITIS; PORPHYROMONAS GINGIVALIS;

EID: 84928569272     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0123448     Document Type: Article

References (51)

1. Kulp A, Kuehn MJ (2010) Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64: 163-184. doi: 10.1146/annurev.micro.091208.073413 PMID: 20825345
2. Biller SJ, Schubotz F, Roggensack SE, Thompson AW, Summons RE, Chisholm SW (2014) Bacterial vesicles in marine ecosystems. Science 343: 183-186. doi: 10.1126/science.1243457 PMID: 24408433
3. Grenier D, Mayrand D (1987) Functional characterization of extracellular vesicles produced by Bacteroides gingivalis. Infect Immun 55: 111-117. PMID: 3539799
4. Lo Storto S, Silvestrini G, Bonucci E (1992) Ultrastructural localization of alkaline and acid phosphatase activities in dental plaque. J Periodontal Res 27: 161-166. PMID: 1608029
5. Deatherage BL, Lara JC, Bergsbaken T, Rassoulian Barrett SL, Lara S, Cookson BT (2009) Biogenesis of bacterial membrane vesicles. Mol Microbiol 72: 1395-1407. doi: 10.1111/j.1365-2958.2009.06731.x PMID: 19432795
6. Bonnington KE, Kuehn MJ (2013) Protein selection and export via outer membrane vesicles. Biochim Biophys Acta.
7. Mashburn LM, Whiteley M (2005) Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437: 422-425. PMID: 16163359
8. Handley PS, Tipler LS (1986) An electron microscope survey of the surface structures and hydrophobicity of oral and non-oral species of the bacterial genus Bacteroides. Arch Oral Biol 31: 325-335. PMID: 2875705
9. Inagaki S, Onishi S, Kuramitsu HK, Sharma A (2006) Porphyromonas gingivalis vesicles enhance attachment, and the leucine-rich repeat BspA protein is required for invasion of epithelial cells by "Tannerella forsythia". Infect Immun 74: 5023-5028. PMID: 16926393
10. Grenier D (2013) Porphyromonas gingivalis Outer Membrane Vesicles Mediate Coaggregation and Piggybacking of Treponema denticola and Lachnoanaerobaculum saburreum. Int J Dent 2013: 305476. doi: 10.1155/2013/305476 PMID: 23365576
11. Kamaguchi A, Nakayama K, Ichiyama S, Nakamura R, Watanabe T, Ohta M, et al. (2003) Effect of Porphyromonas gingivalis vesicles on coaggregation of Staphylococcus aureus to oral microorganisms. Curr Microbiol 47: 485-491. PMID: 14756532
12. Veith PD, Chen YY, Gorasia DG, Chen D, Glew MD, O'Brien-Simpson NM, et al. (2014) Porphyromonas gingivalis Outer Membrane Vesicles Exclusively Contain Outer Membrane and Periplasmic Proteins and Carry a Cargo Enriched with Virulence Factors. J Proteome Res.
13. Nakao R, Takashiba S, Kosono S, Yoshida M, Watanabe H, Ohnishi M, et al. (2014) Effect of Porphyromonas gingivalis outer membrane vesicles on gingipain-mediated detachment of cultured oral epithelial cells and immune responses. Microbes Infect 16: 6-16. doi: 10.1016/j.micinf.2013.10.005 PMID: 24140554
14. Mantri CK, Chen C, Dong X, Goodwin JS, Pratap S, Paromov V, et al. (2014) Fimbriae-mediated outer membrane vesicle production and invasion of Porphyromonas gingivalis. Microbiologyopen.
15. Nakao R, Hasegawa H, Ochiai K, Takashiba S, Ainai A, Ohnishi M, et al. (2011) Outer membrane vesicles of Porphyromonas gingivalis elicit a mucosal immune response. PLoS One 6: e26163. doi: 10.1371/journal.pone.0026163 PMID: 22022548
16. Furuta N, Tsuda K, Omori H, Yoshimori T, Yoshimura F, Amano A (2009) Porphyromonas gingivalis outer membrane vesicles enter human epithelial cells via an endocytic pathway and are sorted to lysosomal compartments. Infect Immun 77: 4187-4196. doi: 10.1128/IAI.00009-09 PMID: 19651865
17. O'Toole GA, Kolter R (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28: 449-461. PMID: 9632250
18. Qi M, Miyakawa H, Kuramitsu HK (2003) Porphyromonas gingivalis induces murine macrophage foam cell formation. Microb Pathog 35: 259-267. PMID: 14580389
19. Velimirov B, Hagemann S (2011) Mobilizable bacterial DNA packaged into membrane vesicles induces serial transduction. Mob Genet Elements 1: 80-81. PMID: 22016850
20. Rumbo C, Fernandez-Moreira E, Merino M, Poza M, Mendez JA, Soares NC, et al. (2011) Horizontal transfer of the OXA-24 carbapenemase gene via outer membrane vesicles: a new mechanism of dissemination of carbapenem resistance genes in Acinetobacter baumannii. Antimicrob Agents Chemother 55: 3084-3090. doi: 10.1128/AAC.00929-10 PMID: 21518847
21. Kolling GL, Matthews KR (1999) Export of virulence genes and Shiga toxin by membrane vesicles of Escherichia coli O157:H7. Appl Environ Microbiol 65: 1843-1848. PMID: 10223967
22. Zheng C, Wu J, Xie H (2011) Differential expression and adherence of Porphyromonas gingivalis FimA genotypes. Mol Oral Microbiol 26: 388-395. doi: 10.1111/j.2041-1014.2011.00626.x PMID: 22053966
23. Maeda K, Nagata H, Nonaka A, Kataoka K, Tanaka M, Shizukuishi S (2004) Oral streptococcal glycer-aldehyde- 3-phosphate dehydrogenase mediates interaction with Porphyromonas gingivalis fimbriae. Microbes Infect 6: 1163-1170. PMID: 15488735
24. Park Y, Simionato MR, Sekiya K, Murakami Y, James D, Chen W, et al. (2005) Short fimbriae of Porphyromonas gingivalis and their role in coadhesion with Streptococcus gordonii. Infect Immun 73: 3983-3989. PMID: 15972485
25. Daep CA, Lamont RJ, Demuth DR (2008) Interaction of Porphyromonas gingivalis with oral streptococci requires a motif that resembles the eukaryotic nuclear receptor box protein-protein interaction domain. Infect Immun 76: 3273-3280. doi: 10.1128/IAI.00366-08 PMID: 18474648
26. Grenier D, Roy S, Chandad F, Plamondon P, Yoshioka M, Nakayama K, et al. (2003) Effect of inactivation of the Arg- and/or Lys-gingipain gene on selected virulence and physiological properties of Porphyromonas gingivalis. Infect Immun 71: 4742-4748. PMID: 12874356
27. Tribble GD, Lamont RJ (2010) Bacterial invasion of epithelial cells and spreading in periodontal tissue. Periodontol 2000 52: 68-83. doi: 10.1111/j.1600-0757.2009.00323.x PMID: 20017796
28. Lamont RJ, Yilmaz O (2002) In or out: the invasiveness of oral bacteria. Periodontol 2000 30: 61-69. PMID: 12236896
29. Yilmaz O, Watanabe K, Lamont RJ (2002) Involvement of integrins in fimbriae-mediated binding and invasion by Porphyromonas gingivalis. Cell Microbiol 4: 305-314. PMID: 12027958
30. Weinberg A, Belton CM, Park Y, Lamont RJ (1997) Role of fimbriae in Porphyromonas gingivalis invasion of gingival epithelial cells. Infect Immun 65: 313-316. PMID: 8975930
31. Hajishengallis G, Lamont RJ (2014) Breaking bad: manipulation of the host response by Porphyromonas gingivalis. Eur J Immunol 44: 328-338. doi: 10.1002/eji.201344202 PMID: 24338806
32. Klieve AV, Yokoyama MT, Forster RJ, Ouwerkerk D, Bain PA, Mawhinney EL (2005) Naturally occurring DNA transfer system associated with membrane vesicles in cellulolytic Ruminococcus spp. of ruminal origin. Appl Environ Microbiol 71: 4248-4253. PMID: 16085810
33. Tribble GD, Rigney TW, Dao DH, Wong CT, Kerr JE, Taylor BE, et al. (2012) Natural competence is a major mechanism for horizontal DNA transfer in the oral pathogen Porphyromonas gingivalis. MBio 3.
34. Kerr JE, Abramian JR, Dao DH, Rigney TW, Fritz J, Pham T, et al. (2014) Genetic Exchange of Fimbrial Alleles Exemplifies the Adaptive Virulence Strategy of Porphyromonas gingivalis. PLoS One 9: e91696. doi: 10.1371/journal.pone.0091696 PMID: 24626479
35. Tribble GD, Lamont GJ, Progulske-Fox A, Lamont RJ (2007) Conjugal transfer of chromosomal DNA contributes to genetic variation in the oral pathogen Porphyromonas gingivalis. J Bacteriol 189: 6382-6388. PMID: 17573478
36. Berleman J, Auer M (2013) The role of bacterial outer membrane vesicles for intra- and interspecies delivery. Environ Microbiol 15: 347-354. doi: 10.1111/1462-2920.12048 PMID: 23227894
37. Tashiro Y, Ichikawa S, Shimizu M, Toyofuku M, Takaya N, Nakajima-Kambe T, et al. (2010) Variation of physiochemical properties and cell association activity of membrane vesicles with growth phase in Pseudomonas aeruginosa. Appl Environ Microbiol 76: 3732-3739. doi: 10.1128/AEM.02794-09 PMID: 20382806
38. Kadurugamuwa JL, Beveridge TJ (1996) Bacteriolytic effect of membrane vesicles from Pseudomonas aeruginosa on other bacteria including pathogens: conceptually new antibiotics. J Bacteriol 178: 2767-2774. PMID: 8631663
39. Libby P (2002) Inflammation in atherosclerosis. Nature 420: 868-874. PMID: 12490960
40. Ross R (1999) Atherosclerosis - an inflammatory disease. N Engl J Med 340: 115-126. PMID: 9887164
41. Reyes L, Herrera D, Kozarov E, Roldan S, Progulske-Fox A (2013) Periodontal bacterial invasion and infection: contribution to atherosclerotic pathology. J Clin Periodontol 40 Suppl 14: S30-50.
42. Beck J, Garcia R, Heiss G, Vokonas PS, Offenbacher S (1996) Periodontal disease and cardiovascular disease. J Periodontol 67: 1123-1137. PMID: 8910831
43. Kozarov E, Sweier D, Shelburne C, Progulske-Fox A, Lopatin D (2006) Detection of bacterial DNA in atheromatous plaques by quantitative PCR. Microbes Infect 8: 687-693. PMID: 16513386
44. Haraszthy VI, Zambon JJ, Trevisan M, Zeid M, Genco RJ (2000) Identification of periodontal pathogens in atheromatous plaques. J Periodontol 71: 1554-1560. PMID: 11063387
45. Koren O, Spor A, Felin J, Fak F, Stombaugh J, Tremaroli V, et al. (2011) Human oral, gut, and plaque microbiota in patients with atherosclerosis. Proc Natl Acad Sci U S A 108 Suppl 1: 4592-4598. doi: 10.1073/pnas.1011383107 PMID: 20937873
46. Elkaim R, Dahan M, Kocgozlu L, Werner S, Kanter D, Kretz JG, et al. (2008) Prevalence of periodontal pathogens in subgingival lesions, atherosclerotic plaques and healthy blood vessels: a preliminary study. J Periodontal Res 43: 224-231. PMID: 18326058
47. Kozarov EV, Dorn BR, Shelburne CE, Dunn WA Jr., Progulske-Fox A (2005) Human atherosclerotic plaque contains viable invasive Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. Arterioscler Thromb Vasc Biol 25: e17-18. PMID: 15662025
48. Rafferty B, Jonsson D, Kalachikov S, Demmer RT, Nowygrod R, Elkind MS, et al. (2011) Impact of monocytic cells on recovery of uncultivable bacteria from atherosclerotic lesions. J Intern Med 270: 273-280. doi: 10.1111/j.1365-2796.2011.02373.x PMID: 21366733
49. Daep CA, Novak EA, Lamont RJ, Demuth DR (2010) Selective substitution of amino acids limits proteolytic cleavage and improves the bioactivity of an anti-biofilm peptide that targets the periodontal pathogen, Porphyromonas gingivalis. Peptides 31: 2173-2178. doi: 10.1016/j.peptides.2010.08.014 PMID: 20800634
50. Silverman RJ, Nobbs AH, Vickerman MM, Barbour ME, Jenkinson HF (2010) Interaction of Candida albicans cell wall Als3 protein with Streptococcus gordonii SspB adhesin promotes development of mixed-species communities. Infect Immun 78: 4644-4652. doi: 10.1128/IAI.00685-10 PMID: 20805332
51. Lin X, Wu J, Xie H (2006) Porphyromonas gingivalis minor fimbriae are required for cell-cell interactions. Infect Immun 74: 6011-6015. PMID: 16988281